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Host immune status affects maturation time in two nematode species – but not as predicted by a simple life-history model

Published online by Cambridge University Press:  17 October 2003

M. A. GUINNEE ,
A. W. GEMMILL ,
B. H. K. CHAN ,
M. E. VINEY  and
A. F. READ
M. A. GUINNEE
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
A. W. GEMMILL
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK Current address: Department of Clinical and Health Psychology, Austin and Repatriation Medical Centre, Repatriation Campus, Banksia Street, Heidelberg West, Victoria 3081, Australia.
B. H. K. CHAN
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
M. E. VINEY
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
A. F. READ
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
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Abstract

In theory, the age at which maturation occurs in parasitic nematodes is inversely related to pre-maturational mortality rate, and cross-species data on mammalian nematodes are consistent with this prediction. Immunity is a major source of parasite mortality and parasites stand to gain sizeable fitness benefits through short-term adjustments of maturation time in response to variation in immune-mediated mortality. The effects of thymus-dependent immune responses on maturation in the nematode parasites Strongyloides ratti and Nippostrongylus brasiliensis were investigated using congenitally thymus-deficient (nude) rats. As compared with worms in normal rats, reproductive maturity of parasites (presence of eggs in utero) in nude rats occurred later in S. ratti but earlier in N. brasiliensis. Immune-mediated differences in maturation time were not associated with differences in worm length. Thymus-dependent immunity had no effect on pre-maturational mortality. Results are discussed in relation to theoretical expectations and possible explanations for the observed patterns in parasite maturation.

Keywords

maturation timeNippostrongylus brasiliensisnude ratsparasitic nematodesStrongyloides ratti
Type
Research Article
Information
Parasitology , Volume 127 , Issue 5 , November 2003 , pp. 507 - 512
Copyright
2003 Cambridge University Press

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References

REFERENCES

AMIRI, P., LOCKSLEY, R. M., PARSLOW, T. G., SAKICK, M., RECTOR, E., RITTER, D. & McKERROW, J. H. (1992). Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature, London 356, 604–607.CrossRefGoogle Scholar
ANDERSON, R. C. ( 1992). Nematode Parasites of Vertebrates: Their Development and Transmission. CAB International, Wallingford, UK.
ANDERSON, R. M. ( 1988). The population biology and genetics of resistance to infection. In Genetics of Resistance to Bacterial and Parasitic Infection (ed. Wakelin, D. & Blackwell, J.), pp. 233–263. Taylor and Francis, London, UK.
CRAWLEY, M. J. ( 1993). GLIM for Ecologists, 1st Edn. Blackwell Scientific Publications, Oxford.
DAVIES, S. J., GROGAN, J. L., BLANK, R. B., LIM, K. C., LOCKSLEY, R. M. & McKERROW, J. H. ( 2001). Modulation of blood fluke development in the liver by hepatic CD4+ lymphocytes. Science 294, 1358–1361.CrossRefGoogle Scholar
DAWKINS, H. J. S., MITCHELL, G. F. & GROVE, D. I. ( 1982). Strongyloides ratti infections in congenitally hypothymic (nude) mice. Australian Journal of Experimental Biology and Medical Science 60, 181–186.CrossRefGoogle Scholar
DE GRISSE, A. T. ( 1969). Redescription ou modifications de quelques techniques utilisées dans l'étude des nematodes phytoparasitaires. Mededelingen Rijksfakulteit Landbouwwetenschappen, Gent 34, 351–369.Google Scholar
GEMMILL, A. W., SKORPING, A. & READ, A. F. ( 1999). Optimal timing of first reproduction in parasitic nematodes. Journal of Evolutionary Biology 12, 1148–1156.CrossRefGoogle Scholar
GEMMILL, A. W., VINEY, M. E. & READ, A. F. ( 1997). Host immune status determines sexuality in a parasitic nematode. Evolution 51, 393–401.CrossRefGoogle Scholar
GEMMILL, A. W., VINEY, M. E. & READ, A. F. ( 2000). The evolutionary ecology of host specificity: experimental studies with Strongyloides ratti. Parasitology 120, 429–437.CrossRefGoogle Scholar
GOLDEN, J. W. & RIDDLE, D. L. ( 1982). A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218, 578–580.CrossRefGoogle Scholar
KASSAI, T. ( 1982). Handbook of Nippostrongylus brasiliensis (Nematode). Commonwealth Agricultural Bureaux, Budapest.
KASSAI, T., TAKÁTS, C. S. & REDL, P. ( 1974). Uniszexuális Nippostrongylus-fertozések immunizáló hatásának kvantitatív vizsgálata patkányban. Parasitologia Hungarica 7, 43–54.Google Scholar
McKAY, D. M., BENJAMIN, M., BACA-ESTRADA, M., D'INCA, R. C. K. & PERDUE, M. H. ( 1995). Role of T lymphocytes in secretory response to an enteric nematode parasite: studies in athymic rats. Digestive Diseases and Sciences 40, 331–337.CrossRefGoogle Scholar
MORAN, N. A. ( 1992). The evolutionary maintenance of alternative phenotypes. American Naturalist 139, 971–989.CrossRefGoogle Scholar
RAVINDRAN, B. ( 2001). Are inflammation and immunological hyperactivity needed for filarial parasite development? Trends in Parasitology 17, 70–73.Google Scholar
RIDDLE, D. L. & ALBERT, P. S. ( 1997). Genetic and environmental regulation of dauer larva development. In C. elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R.), pp. 739–768. Cold Spring Harbor Laboratory Press, New York.
ROFF, D. A. ( 1992). The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York.
SCHEINER, S. M. ( 1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24, 35–68.CrossRefGoogle Scholar
SEINHORST, J. W. ( 1959). A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica 4, 67–69.CrossRefGoogle Scholar
SKORPING, A. & READ, A. F. ( 1998). Drugs and parasites: global experiments in life history evolution? Ecology Letters 1, 10–12.Google Scholar
SMITH, N. C., OVINGTON, K. S. & BRYANT, C. ( 1991). Free radical generation and the course of primary infection with Nippostrongylus brasiliensis in congenitally athymic (nude) rats. Parasite Immunology 13, 571–581.CrossRefGoogle Scholar
STEAR, M. J. & WAKELIN, D. ( 1998). Genetic resistance to parasitic infection. Revue Scientifique et Technique de L'Office International des Epizooties 17, 143–153.CrossRefGoogle Scholar
STEARNS, S. C. ( 1992). Evolution of Life Histories. Oxford University Press, Oxford.
STIBOR, H. & LUNING, J. ( 1994). Predator-induced phenotypic variation in the pattern of growth and reproduction in Daphnia hyalina (Crustacea: Cladocera). Functional Ecology 8, 97–101.CrossRefGoogle Scholar
TINDALL, N. R. & WILSON, P. A. G. ( 1990). A basis to extend the proof of migration routes of immature parasites inside hosts: estimated time of arrival of Nippostrongylus brasiliensis and Strongyloides ratti in the rat. Parasitology 100, 275–280.CrossRefGoogle Scholar
VINEY, M. E. ( 1994). A genetic analysis of reproduction in Strongyloides ratti. Parasitology 109, 511–515.CrossRefGoogle Scholar
VINEY, M. E. ( 1996). Developmental switching in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, Series B. 263, 201–208.CrossRefGoogle Scholar
VINEY, M. E., MATHEWS, B. E. & WALLIKER, D. ( 1992). On the biological and biochemical nature of cloned populations of Strongyloides ratti. Journal of Helminthology 66, 45–52.CrossRefGoogle Scholar
WEIDER, L. J. & PIJANOWSKA, J. ( 1993). Plasticity of Daphnia life histories in response to chemical cues from predators. Oikos 67, 385–392.CrossRefGoogle Scholar